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Ecology of the Threatened Thick-Shelled River Mussel Unio Crassus (Philipsson 1788) with Focus on Mussel-Host Interactions

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Ecology of the Threatened Thick-Shelled River Mussel Unio Crassus (Philipsson 1788) with Focus on Mussel-Host Interactions Ecology of the threatened thick-shelled river mussel Unio crassus (Philipsson 1788) with focus on mussel-host interactions Lea Dominique Schneider Department of Biology Introductory paper No. 11 2014 Ecology of the threatened thick-shelled river mussel Unio crassus (Philipsson 1788) with focus on mussel-host interactions ___________________________________________________________________________ Lea D. Schneider Department of Biology Karlstad University Introductory paper No. 11 2014 Contents 1. Introduction ................................................................................................................................. 3 2. Freshwater mussel ecology – the order Unionoida .................................................................... 5 2.1. Sexual strategies and larval development........................................................................... 5 2.2. The mussel – host-fish relationship ..................................................................................... 8 3. Status and threats to freshwater bivalves................................................................................. 14 4. Conservation strategies ............................................................................................................. 16 5. My doctoral research ................................................................................................................ 17 6. Acknowledgements ................................................................................................................... 19 7. References ................................................................................................................................. 20 2 1. Introduction Freshwater mussels (phylum Mollusca, class Bivalvia) derive from marine species and inhabit a variety of inland waters such as rivers, streams, lakes and ponds worldwide, with the exception of Antarctica. Generally, the most diverse mussel fauna can be found in North America, holding one third of the world’s mussel species (Strayer 2008). Repeated invasions of marine mussels to freshwaters have led to phylogenetically independent bivalve lineages (Graf 2013), resulting in co-existence of non-related freshwater mussel groups such as cyrenids (formerly the corbiculids, Bieler et al. 2010), dreissenids and unionoids (Watters 2001). Mussel colonization of different environments has induced a multitude of mussel life history traits and physiological adaptations to various habitat conditions. The mussel communities in large rivers, for example, are mainly represented by a variety of generalist species that show similar patterns of adaptation to local conditions. For instance, taxa in large rivers with hard sediments often have sculptured shells which facilitate burrowing, while taxa living in soft substrates produce thinner and flattened shells. On the other hand, mussels in headwater streams often have streamlined, unsculptured shells and are usually highly habitat specific (Bauer 2001c). In addition, mussel diversity increases downstream in watersheds, and beta diversity is greatest between headwater streams (Haag and Warren 1998). Mussels are not only affected by habitats, but can also substantially alter the habitats they live in. Mussels bioturbate sediments through pedal (foot) movement (Limm and Power 2011) and together with biodeposition of faeces and pseudofaeces (biodeposits) affect nutrient dynamics and availability in freshwaters (Pusch et al. 2001). Moreover, mussel shells increase pore space in the sediment, contributing to interstitial oxygenation as well as sediment stabilisation. As freshwater mussels are filter feeders, they can improve water clarity, particularly when mussels occur in high densities (Strayer et al. 1994). Furthermore, epiphytic and epizoic organisms use mussel shells as habitat (Vaughn and Hakenkamp 2001). Consequently, the abundance of mussels can greatly contribute to ecosystem functioning and freshwater biodiversity (e.g. Aldridge et al. 2007, Vaughn 2010). The high diversity of life history traits among mussels includes some specialised features. For instance, freshwater mussels belonging to the order Unionoida have a long and complex life cycle (usually > 10 years, Israel 1913), where most species have a larval stage that is dependent on a fish host (Barnhart et al. 2008). The unionoid larvae attach to the gills or skin of the fish, on which they parasitize, from a few days to around one year. After they metamorphose to juvenile mussels they fall off the fish and sink to the sediment. They then bury themselves into the sediment, completing development to reproducing adults within a few to approximately 15-20 years (Fig 1). Such specialized life cycles can, although adaptive, face a number of challenges, as both fish community structure and habitat conditions must meet the needs of each life-cycle stage of the mussels (Strayer et al. 2004, Vaughn and Taylor 2000, Österling et al. 2008). 3 Fig. 1 Life cycle of Unio crassus with the minnow (Phoxinus phoxinus) acting as a host fish for the mussel larvae (glochidia). © UC4LIFE The freshwater unionid bivalves are one of the most threatened groups of organisms on earth. The global decline of these mussel species is probably related to both anthropogenic activities and the complex life history traits of these mussels (Bogan 2008). For some species, every life stage is negatively affected (Österling 2014). A lack of suitable fish hosts can impair mussel recruitment, affecting population density, potentially leading to extinction (Zale and Neves 1982, Arvidsson et al. 2012). Fish composition has been largely affected by anthropogenic habitat alteration since the industrial revolution. Freshwater mussels are also sensitive to habitat modification, water pollution, land-use change, exotic species introductions and overharvesting (Zahner-Meike and Hanson 2001, Bauer and Wächtler 2001, Strayer et al. 2004, Österling et al. 2008, Österling et al. 2010). Freshwater mussels have been described as keystone species in freshwater ecosystems, with high conservation value (e.g. Vaughn and Hakenkamp 2001, Gutiérrez et al. 2003). To be able to preserve the mussel fauna worldwide, as well as their hosts, direct conservation strategies need to be established (Geist 2010). Therefore, knowledge about the interaction between individual mussel species and their habitats is of utmost importance, and particularly so the co-evolutionary link between mussels and fish hosts. Host fish assemblage and abundance strongly determine mussel abundance and community structure (Vaughn and Taylor 2000, Arvidsson et al. 2013). Thus, there is great need to evaluate the adaptive mechanisms behind the parasite-host interactions, something that hitherto only has been 4 understood for a few of the thousand freshwater mussel species existing worldwide (Strayer et al. 2004). The objective of this introductory essay is to review the mussel – host-fish interactions of unionoid mussels, and relate these general interactions to the threatened thick-shelled river mussel Unio crassus (Philipsson 1788), the target species of my PhD thesis. Therefore, the species’ life history traits are discussed in a broad context of freshwater mussel ecology. As U. crassus is the most threatened European unionoid (Lundberg 2007), its status and threats are summed up to be able to relate to essential research and conservation of the species. So far, the question of the relationship between U. crassus and its hosts has only been addressed a few times, mostly in Germany, the Czech Republic and Luxemburg. Here, the European minnow (Phoxinus phoxinus), the European chub (Squalius cephalus) and the bullhead (Cottus gobio) have been identified as major host fish species (e.g. Bednarczuk 1986, Maaß 1987, Hochwald 1997, Thielen 2011, Douda et al. 2012, Taeubert et al. 2012a). However, it has also been shown that the host fish use varies between different drainage areas and their fish populations (e.g. Hochwald and Bauer 1990, Taeubert et al. 2012a). Wengström (2009), for example, reported on mussel population with successful recruitment where minnow, chub and bullhead were absent. This indicates a need for further research clarifying the relationship between mussels and fish for the entire mussel distribution area, so that one can establish conservation strategies for mussels and fish. My doctoral research will be presented at the end of this introductory essay. 2. Freshwater mussel ecology – the order Unionoida In this chapter, I provide an overview of the general life cycle of freshwater mussels, along with specifications for each life cycle stage for U. crassus. First, I discuss sexual strategies and larval development which secondly is followed by a discussion of the mussel – host-fish relationship. 2.1. Sexual strategies and larval development Having derived from marine mussel species, all three freshwater mussel lineages (cyrenids, formerly the corbiculids, Bieler et al. 2010; dreissenids and unionids) developed their mode of reproduction from oviparous broadcast spawning towards ovoviviparity and even euviviparity. Thus, in contrast to their marine ancestors that cast out sperms and eggs separately in free flowing water resulting in external egg fertilization and development of planktonic veliger larvae, freshwater mussels adopted parental care (i.e. brooding). Accordingly, female mussels keep their eggs in the marsupium for fertilization by filtered sperms. Egg development in euviviparous mussel species, mostly
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